Interactions of Tomato and Botrytis cinerea Genetic Diversity: Parsing the Contributions of Host Differentiation, Domestication, and Pathogen Variation.

Although the impacts of crop domestication on specialist pathogens are well known, less is known about the interaction of crop variation and generalist pathogens. To study how genetic variation within a crop affects plant resistance to generalist pathogens, we infected a collection of wild and domesticated tomato accessions with a genetically diverse population of the generalist pathogen Botrytis cinerea We quantified variation in lesion size of 97 B. cinerea genotypes (isolates) on six domesticated tomato genotypes (Solanum lycopersicum) and six wild tomato genotypes (Solanum pimpinellifolium). Lesion size was significantly affected by large effects of the host and pathogen's genotype, with a much smaller contribution of domestication. This pathogen collection also enables genome-wide association mapping of B. cinerea Genome-wide association mapping of the pathogen showed that virulence is highly polygenic and involves a diversity of mechanisms. Breeding against this pathogen would likely require the use of diverse isolates to capture all possible mechanisms. Critically, we identified a subset of B. cinerea genes where allelic variation was linked to altered virulence against wild versus domesticated tomato, as well as loci that could handle both groups. This generalist pathogen already has a large collection of allelic variation that must be considered when designing a breeding program.

Digital Imaging Combined with Genome-Wide Association Mapping Links Loci to Plant-Pathogen Interaction Traits.

Plant resistance to generalist pathogens with broad host ranges, such as Botrytis cinerea (Botrytis), is typically quantitative and highly polygenic. Recent studies have begun to elucidate the molecular genetic basis of plant-pathogen interactions using commonly measured traits, including lesion size and/or pathogen biomass. However, with the advent of digital imaging and high-throughput phenomics, there are a large number of additional traits available to study quantitative resistance. In this study, we used high-throughput digital imaging analysis to investigate previously poorly characterized visual traits of plant-pathogen interactions related to disease resistance using the Arabidopsis (Arabidopsis thaliana)/Botrytis pathosystem. From a large collection of visual lesion trait measurements, we focused on color, shape, and size to test how these aspects of the Arabidopsis/Botrytis interaction are genetically related. Through genome-wide association mapping in Arabidopsis, we show that lesion color and shape are genetically separable traits associated with plant disease resistance. Moreover, by employing defined mutants in 23 candidate genes identified from the genome-wide association mapping, we demonstrate links between loci and each of the different plant-pathogen interaction traits. These results expand our understanding of the functional mechanisms driving plant disease resistance.

Quantitative interactions: the disease outcome of Botrytis cinerea across the plant kingdom.

Botrytis cinerea is a fungal pathogen that causes necrotic disease on more than a thousand known hosts widely spread across the plant kingdom. How B. cinerea interacts with such extensive host diversity remains largely unknown. To address this question, we generated an infectivity matrix of 98 strains of B. cinerea on 90 genotypes representing eight host plants. This experimental infectivity matrix revealed that the disease outcome is largely explained by variations in either the host resistance or pathogen virulence. However, the specific interactions between host and pathogen account for 16% of the disease outcome. Furthermore, the disease outcomes cluster among genotypes of a species but are independent of the relatedness between hosts. When analyzing the host specificity and virulence of B. cinerea, generalist strains are predominant. In this fungal necrotroph, specialization may happen by a loss in virulence on most hosts rather than an increase of virulence on a specific host. To uncover the genetic architecture of Botrytis host specificity and virulence, a genome-wide association study (GWAS) was performed and revealed up to 1492 genes of interest. The genetic architecture of these traits is widespread across the B. cinerea genome. The complexity of the disease outcome might be explained by hundreds of functionally diverse genes putatively involved in adjusting the infection to diverse hosts.